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Cell damage induced by polybrominated diphenyl ethers on Chironomus sancticaroli (Diptera: Chironomidae)

Abstract

Histological effects of polybrominated diphenyl ethers (PBDEs) were observed in Chironomus sancticaroli larvae which underwent acute exposure. 2,2′,4-triBDE (BDE-17), 2,2′,4,4′-tetraBDE (BDE-47) and 2,2′,4,4′,5-pentaBDE (BDE-99) were evaluated at 0.5, 2.0 and 20 μg L-1. Cytoplasm vacuolisation of oenocytes was observed in the larvae exposed to BDE-17 and BDE-47. Cuénot cells were disrupted at the brush border as an effect of the three evaluated congeners highlighting BDE-47 at 2.0 μg L-1; 60% of larvae displayed this disruption. The midgut showed changes in the morphology of apex cells located next to the lumen of region I exposed to BDE-17 and BDE-47, while BDE-99 induced a narrowing of the lumen diameter. Significant cytoplasm vacuolisation of the larvae exposed to BDE-47 and BDE-99 was observed in region II of the midgut. Salivary glands showed acidophilic granules in the cytoplasm exposed to BDE-17 and BDE-47. The results showed that the tissues of C. sancticaroli were sensitive to flame retardants; these histopathologies can compromise the health and physiology of this organism, highlighting the concern with the presence of PBDEs in freshwater sediments.

Keywords:
Cuénot cells; Flame retardants; Midge; Oenocytes; salivary glands

Introduction

Chironomidae are the most common group of insects present in freshwater habitats. As sediment-dwelling organisms in the larval stages, they change the structure and properties of the substrate and act as significant organic matter recyclers (Armitage et al., 1995Armitage, P. D., Pinder, L. C., Cranston, P., 1995. The Chironomidae: The Biology and Ecology of Non-bitting Midges, Chapman & Hall, London, UK.). In addition to their ecological ubiquity and species richness, chironomid larvae are capable of transferring contaminants present in sediment from larvae to adults (Reinhold et al., 1999Reinhold, J. O., Hendriks, A. J., Slager, L. K., Ohm, M., 1999. Transfer of microcontaminants from sediment to chironomids, and the risk for the Pond bat Myotis dasycneme (Chiroptera) preying on them. Aquat. Ecol. 33 (4), 363-376. https://doi.org/10.1023/A:1009958028204.
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) and likewise play an important role transporting contaminants through the food web that can modify ecosystem health (Clements et al., 1994Clements, W. H., Oris, J. T., Wissing, T. E., 1994. Accumulation and food chain transfer of fluoranthene and benzo[a]pyrene in Chironomus riparius and Lepomis macrochirus. Arch. Environ. Contam. Toxicol. 26 (3), 261-266. https://doi.org/10.1007/BF00203550.
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). These characteristics as well as their short lifecycle and ability to be easily cultured in the laboratory are advantages that make them good model organisms to indicate the quality of freshwater and sediment environments (Armitage et al., 1995Armitage, P. D., Pinder, L. C., Cranston, P., 1995. The Chironomidae: The Biology and Ecology of Non-bitting Midges, Chapman & Hall, London, UK.; OECD, 2010OECD, 2010. Sediment-water Chironomid life-cycle toxicity test using spiked water or spiked sediment. In: OECD, OECD Guidelines for the Testing of Chemicals, Section 2. OECD, Paris, pp. 1-29.; Serra et al., 2017Serra, S. R. Q., Graça, M. A. S., Dolédec, S., Feio, M. J., 2017. Chironomidae traits and life history strategies as indicators of anthropogenic disturbance. Environ. Monit. Assess. 189, 326. https://doi.org/10.1007/s10661-017-6027-y.
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). Chironomus sancticaroli Strixino-Strixino, 1981, including its synonym Chironomus xanthus, Rempel, 1939, is endemic to the Neotropical region (Trivinho-Strixino, 2011Trivinho-Strixino, S. 2011. Chironomidae (Insecta, Diptera, Nematocera) do Estado de São Paulo, Sudeste do Brasil. Biota Neotrop. 11, 675-684.) and has been identified as an appropriate model to estimate local environmental conditions.

Among the chemicals in products (CiPs) which are emerging contaminants of public health concern, the polybrominated diphenyl ethers (PBDEs) stand out. These synthetic chemicals are incorporated either through reaction or addition into household and commercial polymer-based products like textiles, electronic devices and furniture to reduce flammability in case of fire (De Wit, 2002De Wit, C. A. 2002. An overview of brominated flame retardants in the environment. Chemosphere. 46 (5), 583-624. https://doi.org/10.1016/S0045-6535(01)00225-9.
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; WHO, 1997WHO, 1997. Flame Retardants: A General Introduction, Environmental Health Criteria. No. 192. World Health Organization, Geneva.). It is estimated that plastic materials flameproofed by PBDEs can contain between 0.5 to 30% of PBDE of their total mass (Alaee et al., 2003Alaee, M., Arias, P., Sjödin, A., Bergman, Å., 2003. An overview of commercially used brominated flame retardants, their applications, their use patterns in different countries/regions and possible modes of release. Environ. Int. 29 (6), 683-689. https://doi.org/10.1016/S0160-4120(03)00121-1.
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). PBDEs can leach out into the environment during their production, use, waste disposal or during the recycling process (Rahman et al., 2001Rahman, F., Langford, K. H., Scrimshaw, M. D., Lester, J. N., 2001. Polybrominated Diphenyl Ether (PBDE) flame retardants. Sci. Total Environ. 275 (1-3), 1-17. https://doi.org/10.1016/S0048-9697(01)00852-X.
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; Salvadó et al., 2016Salvadó, J. A., Sobek, A., Carrizo, D., Gustafsson, Ö., 2016. Observation-based assessment of PBDE loads in Arctic Ocean waters. Environ. Sci. Technol. 50 (5), 2236-2245. https://doi.org/10.1021/acs.est.5b05687.
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). In addition, there are sources of PBDEs emission from combustion of waste electrical and electronic equipment (WEEE) and e-waste ignition (Redfern et al., 2017Redfern, F. M., Lee, W. J., Yan, P., Mwangi, J. K., Wang, L. C., Shih, C. H., 2017. Overview and perspectives on emissions of polybrominated diphenyl ethers on a global basis: Evaporative and fugitive releases from commercial PBDE mixtures and emissions from combustion sources. Aerosol Air Qual. Res. 17 (5), 1117-1131. https://doi.org/10.4209/aaqr.2016.12.0579.
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). Leaching rate of PBDEs that are covalently bonded to the polymer is lower than those added or mixed to the product (De Wit, 2002De Wit, C. A. 2002. An overview of brominated flame retardants in the environment. Chemosphere. 46 (5), 583-624. https://doi.org/10.1016/S0045-6535(01)00225-9.
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). It has been estimated that the cumulative historical production of mixtures containing PBDEs varied from 100 to 1600 kilotonnes (Abbasi et al., 2019Abbasi, G., Li, L., Breivik, K., 2019. Global historical stocks and emissions of PBDEs. Environ. Sci. Technol. 53 (11), 6330-6340. https://doi.org/10.1021/acs.est.8b07032.
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).

Depending on their average bromine content, 209 PBDEs can be produced. They used to be commercialised in the formulation of penta-BDE, octa-BDE and deca-BDE (Alaee et al., 2003Alaee, M., Arias, P., Sjödin, A., Bergman, Å., 2003. An overview of commercially used brominated flame retardants, their applications, their use patterns in different countries/regions and possible modes of release. Environ. Int. 29 (6), 683-689. https://doi.org/10.1016/S0160-4120(03)00121-1.
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; WHO, 1997WHO, 1997. Flame Retardants: A General Introduction, Environmental Health Criteria. No. 192. World Health Organization, Geneva.). Currently, BDE-47 (2,2’,4,4’-tetrabromodiphenyl ether) and BDE-99 (2,2’,4,4’,5-pentabromodiphenyl ether) are most frequently encountered in environmental samples and animal tissues (Cunha et al., 2010Cunha, S. C., Kalachova, K., Pulkrabova, J., Fernandes, J. O., Oliveira, M. B. P. P., Alves, A., Hajslova, J., 2010. Polybrominated diphenyl ethers (PBDEs) contents in house and car dust of Portugal by pressurized liquid extraction (PLE) and gas chromatography-mass spectrometry (GC-MS). Chemosphere 78 (10), 1263-1271. https://doi.org/10.1016/j.chemosphere.2009.12.037.
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; Kalantzi et al., 2009Kalantzi, O. I., Brown, F. R., Caleffi, M., Goth-Goldstein, R., Petreas, M., 2009. Polybrominated diphenyl ethers and polychlorinated biphenyls in human breast adipose samples from Brazil. Environ. Int. 35 (1), 113-117. https://doi.org/10.1016/j.envint.2008.09.008.
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). Nevertheless, BDE-17 (2,2’,4-Tribromodiphenyl ether) has also been detected (Christiansson et al., 2008Christiansson, A., Hovander, L., Athanassiadis, I., Jakobsson, K., Bergman, Å., 2008. Polybrominated diphenyl ethers in aircraft cabins: A source of human exposure? Chemosphere 73 (10), 1654-1660. https://doi.org/10.1016/j.chemosphere.2008.07.071.
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).

Even though some of the formulations of PBDEs were withdrawn from the market and banned by the Stockholm Convention, they are still present in environmental compartments (European Union, 2004European Union, 2004. Directive 2003/11/EC of the European Parliament and of the Council of 6 February 2003 Amending for the 24th Time Council Directive 76/769/ EEC Relating to Restrictions on the Marketing and Use of Certain Dangerous Substances and Preparations. Available in: http://op.europa.eu/en/publication-detail/-/publication/3a8d2aa2-2d34-4bec-bef2-3f45e17ab09b/language-en (accessed. 19 July 2018).
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; GLCC, 2003GLCC, 2003. Press release: Thanks to New Product Technology, Great Lakes Will Cease Production of penta-PBDE Flame Retardant by End of 2004. Available in: www.greatlakes.com (accessed 22 April 2018).
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; Stockholm Convention, 2009Stockholm Convention, 2009. Available in: http://chm.pops.int/TheConvention/ThePOPs/TheNewPOPs/tabid/2511/Default.aspx (accessed 20 March 2018).
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). The PBDE levels in the environment depend on factors that include local anthropogenic activities, environmental photodegradation and presence of degrading microorganisms (Shi et al., 2015Shi, S. X., Huang, Y. R., Zhou, L., Zhang, L. F., Dong, L., Yang, W. L., Zhang, X. L., 2015. Changes of polybrominated diphenyl ethers and polychlorinated biphenyls in surface soils from urban agglomeration of the Yangtze River Delta, in China between 2003 and 2012. Environ. Sci. Pollut. Res. Int. 22, 9766.; Song et al., 2015Song, M., Luo, C., Li, F., Jiang, L., Wang, Y., Zhang, D., Zhang, G., 2015. Anaerobic degradation of Polychlorinated Biphenyls (PCBs) and Polychlorinated Biphenyls Ethers (PBDEs), and microbial community dynamics of electronic waste-contaminated soil. Sci. Total Environ. 502, 426-433. https://doi.org/10.1016/j.scitotenv.2014.09.045.
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). Cristale et al. (2019)Cristale, J., Gomes, T., Belé, A., Lacorte, S., Rodrigues de Marchi, M. R., 2019. Occurrence of flame retardants in landfills: A case study in Brazil. Environ. Res. 168, 420-427. https://doi.org/10.1016/j.envres.2018.10.010.
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measured PBDEs levels in a Brazilian landfill describing concentrations in soil ranging from 3 to 715 ng g-1 and in dust from 11 to 3500 ng g-1. Similarly, levels of PBDEs in dust from houses ranged from 8 to 407 ng g-1. A different study showed that the maximum level of PBEs concentration in sediment samples from a groundwater water supply in Brazil was 5.4 ng g-1 (Ferrari et al., 2019Ferrari, R. S., Souza, A. O., Annunciação, D. L. R., Sodré, F. F., Dorta, D. J., 2019. Assessing surface sediment contamination by PBDE in a recharge point of Guarani Aquifer in Ribeirão Preto, Brazil. Water 11 (8), 1601. https://doi.org/10.3390/w11081601.
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). Considering biological samples, PBDEs have been detected in species of fish, mussels and dolphins from Brazil (Silva et al., 2013Silva, G. S. F., Brüning, I. M. R. A., Montone, R. C., Taniguchi, S., Cascaes, M. J., Dias, P. S., Lavandier, R. C., 2013. Polybrominated Diphenyl Ethers (PBDES) and Polychlorinated Biphenyls (PCBS) in mussels and two fish species from the estuary of the Guanabara Bay, Southeastern Brazil. Bull. Environ. Contam. Toxicol. 91 (3), 261-266.; Magalhães et al., 2017Magalhães, C., Taniguchi, S., Lourenço, R., Montone, R., 2017. Organochlorine pesticides, PCBs, and PBDEs in liver and muscle tissues of Paralonchurus brasiliensis, Trichiurus lepturus and Cathorops spixii in Santos Bay and surrounding area, São Paulo, Brazil. Reg. Stud. Mar. Sci. 16, 42-48.; Quinete et al., 2011Quinete, N., Lavandier, R., Dias, P., Taniguchi, S., Montone, R., Moreira, I., 2011. Specific profiles of polybrominated diphenylethers (PBDEs) and polychlorinated biphenyls (PCBs) in fish and tucuxi dolphins from the estuary of Paraíba do Sul River, Southeastern Brazil. Mar. Pollut. Bull. 62 (2), 440-446.; Yogui et al., 2011Yogui, G. T., Santos, M. C. O., Bertozzi, C. P., Sericano, J. L., Montone, R. C., 2011. PBDEs in the blubber of marine mammals from coastal areas of São Paulo, Brazil, southwestern Atlantic. Mar. Pollut. Bull. 62 (12), 2666-2670.).

Due to their physico-chemical properties, PBDEs are persistent and prone to long-range atmospheric transport. Therefore, they have been detected in aquatic and terrestrial organisms, including human blood and breast milk (De Wit et al., 2010De Wit, C. A., Herzke, D., Vorkamp, K., 2010. Brominated flame retardants in the Arctic environment - trends and new candidates. Sci. Total Environ. 408 (15), 2885-2918. https://doi.org/10.1016/j.scitotenv.2009.08.037.
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; Dornbos et al., 2015Dornbos, P., Chernyak, S., Rutkiewicz, J., Cooley, T., Strom, S., Batterman, S., Basu, N., 2015. Hepatic polybrominated diphenyl ether (PBDE) levels in Wisconsin river otters (Lontra canadensis) and Michigan bald eagles (Haliaeetus leucocephalus). J. Great Lakes Res. 41 (1), 222-227. https://doi.org/10.1016/j.jglr.2014.12.023.
https://doi.org/10.1016/j.jglr.2014.12.0...
; Hurley et al., 2017Hurley, S., Goldberg, D., Nelson, D. O., Guo, W., Wang, Y., Baek, H.-G., Park, J.-S., Petreas, M., Bernstein, L., Anton-Culver, H., Reynolds, P., 2017. Temporal evaluation of polybrominated diphenyl ether (PBDE) serum levels in middle-aged and older California women, 2011-2015. Environ. Sci. Technol. 51 (8), 4697-4704. https://doi.org/10.1021/acs.est.7b00565.
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; Zheng et al., 2016Zheng, B., Zhao, X., Ni, X., Ben, Y., Guo, R., An, L., 2016. Bioaccumulation characteristics of polybrominated diphenyl ethers in the marine food web of Bohai Bay. Chemosphere 150, 424-430. https://doi.org/10.1016/J.CHEMOSPHERE.2016.01.110.
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). Several studies have shown that some congeners modify developmental and reproductive systems (Dufault et al., 2005Dufault, C., Poles, G., Driscoll, L. L., 2005. Brief postnatal PBDE exposure alters learning and the cholinergic modulation of attention in Rats. Toxicol. Sci. 88 (1), 172-180. https://doi.org/10.1093/toxsci/kfi285.
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; Usenko et al., 2011Usenko, C. Y., Robinson, E. M., Usenko, S., Brooks, B. W., Bruce, E. D., 2011. PBDE developmental effects on embryonic zebrafish. Environ. Toxicol. Chem. 30 (8), 1865-1872. https://doi.org/10.1002/etc.570.
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), are neurotoxic (Costa et al., 2014Costa, L. G., de Laat, R., Tagliaferri, S., Pellacani, C., 2014. A mechanistic view of polybrominated diphenyl ether (PBDE) developmental neurotoxicity. Toxicol. Lett. 230 (2), 282-294. https://doi.org/10.1016/j.toxlet.2013.11.011.
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; Zheng et al., 2017Zheng, S., Liu, C., Huang, Y., Bao, M., Huang, Y., Wu, K., 2017. Effects of 2,2′,4,4′-tetrabromodiphenyl ether on neurobehavior and memory change and bcl-2, c-fos, grin1b and lingo1b gene expression in male zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 333, 10-16. https://doi.org/10.1016/J.TAAP.2017.08.004.
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) and carcinogenic (Man et al., 2011Man, Y. B., Lopez, B. N., Wang, H. S., Leung, A. O. W., Chow, K. L., Wong, M. H., 2011. Cancer risk assessment of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) in former agricultural soils of Hong Kong. J. Hazard. Mater. 195, 92-99. https://doi.org/10.1016/j.jhazmat.2011.08.010.
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; Ward et al., 2014Ward, M., Colt, J., Deziel, N., Whitehead, T., Reynolds, P., Gunier, R., Nishioka, M., Dahl, G., Rappaport, S., Buffer, P., Metayer, C., 2014. Residential levels of polybrominated diphenyl ethers and risk of childhood acute lymphoblastic leukemia in California. Environ. Health Perspect. 122 (10), 1110-1116. https://doi.org/10.1289/ehp.1307602.
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) and induce endocrine disruption (Fernie et al., 2005Fernie, K. J., Shutt, J. L., Mayne, G., Hoffman, D., Letcher, R. J., Drouillard, K. G., Ritchie, I. J., 2005. Exposure to polybrominated diphenyl ethers (PBDEs): changes in thyroid, vitamin A, glutathione homeostasis, and oxidative stress in American kestrels (Falco sparverius). Toxicol. Sci. 88, 375-383. https://doi.org/10.1093/toxsci/kfi295.
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; Metcalfe et al., 2013Metcalfe, C. D., Kleywegt, S., Letcher, R. J., Topp, E., Wagh, P., Trudeau, V. L., Moon, T. W., 2013. A multi-assay screening approach for assessment of endocrine-active contaminants in wastewater effluent samples. Sci. Total Environ. 454-455, 132-140. https://doi.org/10.1016/j.scitotenv.2013.02.074.
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). Studies related to the potential effects of PBDEs on population or community levels are rare, although it has been described that the presence of PBDEs in sediments can influence recruitment and fitness of marine benthic communities, specifically, polychaetes once PBDEs alter their settlement in a habitat (Lam et al., 2010Lam, C., Neumann, R., Shin, P. K., Au, D. W. T., Qian, P. Y., Wu, R. S. S., 2010. Polybrominated Diphenylethers (PBDEs) alter larval settlement of marine benthic polychaetes. Environ. Sci. Technol. 44 (18), 7130-7137.).

The health status of a single organism as a result of sublethal effects caused by environmental contaminants can be measured at sub-cellular level allowing the recognition of target organs which in turn can be identified by histological analyses. The alterations can help to predict changes at higher levels of the species that make up the ecosystems affected by the contaminants (Hinton et al., 1992Hinton, D. E., Baumann, P. C., Gardner, G. R., Hawkins, W. E., Hendricks, J. D., Murchelano, R. A., Okihiro, M. S., 1992. Histopathologic Biomarkers. In: Huggett, R.J., Kimerle, R.A., Mehrie, J.P.M., Bergman, H.L. (Eds.), Biomarkers: Biochemical Physiological and Histological Markers of Anthropogenic Stress. Taylor & Francis, Boca Raton, pp. 155-211.; Myers & Fournie, 2002Myers, M. S., Fournie, J. W., 2002. Histological biomarkers as integrators of anthropogenic and environmental stressors. In: Marshall, A. (Ed.), Bioindicators of Stress in Aquatic Organisms. Wiley and Sons, Florida, pp. 221-287.). In particular, some cells or structures of chironomid larvae can be histologically analyzed to identify the effects of contaminants due to their importance in the physiology of the organism. For instance, oenocytes cells are associated with detoxification processes of larvae (Locke, 1969Locke, M. 1969. The ultrastructure of the oenocytes in the molt/intermolt cycle of an insect. Tissue Cell 1, 103-154.; Lycett et al., 2006Lycett, G. J., McLaughlin, L. A., Ranson, H., Hemingway, J., Kafatos, F. C., Loukeris, T. G., Paine, M. J. I., 2006. Anopheles gambiae P450 reductase is highly expressed in oenocytes and in vivo knockdown increases permethrin susceptibility. Insect Mol. Biol. 15 (3), 321-327. https://doi.org/10.1111/j.1365-2583.2006.00647.x.
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) and are related to the formation of an impermeable surface in the epicuticle (Roma et al., 2010Roma, G. C., Bueno, O. C., Camargo-Mathias, M. I., 2010. Morpho-physiological analysis of the insect fat body: A review. Micron 41 (5), 395-401. https://doi.org/10.1016/J.MICRON.2009.12.007.
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). Additionally, oenocytes contribute to lipid metabolism (Gutierrez et al., 2007Gutierrez, E., Wiggins, D., Fielding, B., Gould, A. P., 2007. Specialized hepatocyte-like cells regulate Drosophila lipid metabolism. Nature 445, 275-280. https://doi.org/10.1038/nature05382.
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) and production of hormones such as ecdysteroids that induce the metamorphosis and activate the renovation of the larval tissues (Rachinsky et al., 1990Rachinsky, A., Strambi, C., Strambi, A., Hartfelder, K., 1990. Caste and metamorphosis: hemolymph titers of juvenile hormone and ecdysteroids in last instar honeybee larvae. Gen. Comp. Endocrinol. 79 (1), 31-38. https://doi.org/10.1016/0016-6480(90)90085-Z.
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; Romer & Bressel, 1994Romer, F., Bressel, H. U., 1994. Secretion and metabolism of ecdysteroids by oenocyte-fat body complexes (OEFC) in adult males of Gryllus bimaculatus DEG (Insecta). Z. Naturforsch. C Biosci. 49 (11-12), 871-880. https://doi.org/10.1515/znc-1994-11-1224.
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), and they influence the storage site of haemoglobins (Bergtrom et al., 1976Bergtrom, G., Laufer, H., Rogers, R., 1976. Fat body: a site of hemoglobin synthesis in Chironomus thummi (diptera). J. Cell Biol. 69, 264-274. https://doi.org/10.1083/JCB.69.2.264.
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).

Similarly, Cuénot cells, which are aggregates of oesophageal projection units, are responsible for producing the peritrophic matrix cells (Pierson, 1956Pierson, M. 1956. Contribution a l’histologie de l’appareil digestif de Chironomus plumosus L. Ann. des Sci. Nat. Zoolgie Biol. Anim. 18, 107-122.; Richardi et al., 2015Richardi, V. S., Vicentini, M., Rebechi, D., Fávaro, L. F., Navarro-Silva, M. A., Richardi, V. S., Vicentini, M., Rebechi, D., Fávaro, L. F., Navarro-Silva, M. A., 2015. Morpho-histological characterization of immature of the bioindicator midge Chironomus sancticaroli Strixino and Strixino (Diptera, Chironomidae). Rev. Bras. Entomol. 59, 240-250. https://doi.org/10.1016/j.rbe.2015.07.003.
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). The salivary glands of chironomids are responsible for producing structural proteins that modulate the silk production involved in filter feeding and construction of housing tubes during the larval and prepupal stages (Wallace & Merritt, 1980Wallace, J. B., Merritt, R. W., 1980. Filter-feeding ecology of aquatic insects. Annu. Rev. Entomol. 25, 103-132. https://doi.org/10.1146/annurev.en.25.010180.000535.
https://doi.org/10.1146/annurev.en.25.01...
; Wieslander, 1994Wieslander, L. 1994. The Balbiani ring multigene family: coding repetitive sequences and evolution of a tissue-specific cell function. Prog. Nucleic Acid Res. Mol. Biol. 48, 275-313.). Malpighian tubules that lie freely in the body cavity, are related to the homeostasis regulation and removal of nitrogenous waste products and toxic substances, and some are also linked to the immune defence of insects (Beyenbach et al., 2010Beyenbach, K. W., Skaer, H., Dow, J. A. T., 2010. The developmental, molecular, and transport biology of Malpighian tubules. Annu. Rev. Entomol. 55, 351-374. https://doi.org/10.1146/annurev-ento-112408-085512.
https://doi.org/10.1146/annurev-ento-112...
; Chapman, 2013Chapman, R. F., 2013. Excretion and salt and water regulation. In: Simpson, S., Douglas, A. (Eds.), The Insects: Structure and Function. Cambridge University Press, New York, pp. 546-584.; Wigglesworth, 1972Wigglesworth, V. B. 1972. Excretion. In: The Principles of Insect Physiology. Springer, Netherlands, pp. 553-592. https://doi.org/10.1007/978-94-009-5973-6_12
https://doi.org/10.1007/978-94-009-5973-...
). Because interaction with contaminants occurs after ingestion of food or water, we considered that the midgut should also be considered a target site for our analyses.

Taking all of the aforementioned aspects into account and the little information available on the influence of PBDEs in tissues of chironomids, the goal of this study was to assess the effects of BDE-17, BDE-47 and BDE-99 on different tissues of fourth instar larvae of C. sancticaroli after short-term exposure.

Materials and methods

Larvae of Chironomus sancticaroli were obtained from the colony of the Laboratory of Morphology and Physiology of Culicidae and Chironomidae (LAMFIC2), maintained at the Federal University of Paraná (UFPR). The colony was kept in aerated aquaria following the protocol of Maier et al. (1990)Maier, K. J., Kosalwat, P., Knight, A. W., 1990. Culture of Chironomus decorus (Diptera: Chironomidae) and the effect of temperature on its life history. Environ. Entomol. 19, 1681-1688. under 25ºC ± 2, 80% relative humidity and photophase:scotophase (12:12). Larvae were fed three times a week with DogChow® (Nestlé – Purina, Switzerland). Voucher specimens of this colony are in the Entomology Museum of the Zoology Department at the Federal University of Paraná (DZUP) with accession numbers 249269 to 249276.

To perform the bioassays, freshly laid egg masses from the colony were transferred to trays containing reconstituted water with 1.2 mg L-1 hydrated CaSO4, 0.08 mg L-1 KCl, 2.44 mg L-1 MgSO47H2O, 1.92 mg L-1 Na2CO3, conductivity of 160 μS cm-1, pH 7.2 and hardness 16 mg L-1. Larvae were fed with TetraMin® fish three times per week and constant aeration was maintained until they reached the fourth-instar, when they were exposed to PDBEs.

Nine bioassays were conducted in glass vessels containing ten larvae each, 50 mL of reconstituted water and 13 g of sand 50-70 mesh Sigma®. BDE-17, BDE-47 and BDE-99 were tested at 0.5, 2.0 and 20 μg L-1 after 48 hours of exposure. Two acetone and two water replicates were considered control groups. In total, 130 larvae were exposed. Bioassays were conducted in a BOD chamber under 25±2 °C, 80% relative humidity and a photoperiod of 12 hours. Additionally, temperature, conductivity, pH and dissolved oxygen concentrations were determined at 0 hours and 48 hours after exposure.

Experimental solutions

Analytical grade standards of BDE-17 (CAS No. 147217-75), BDE- 47 (CAS No 5436-43-1) and BDE-99 (CAS No 60348-60-9) in isooctane (50 μg mL-1) were purchased from Accustandard® (New Heaven, CT). Stock solutions at 1000 μg L-1 for dosing at 0.5 and 2.0 μg L-1 were prepared in acetone and stored in amber glass vials at -20°C until the bioassays were initiated. Larvae exposed to 20 μg L-1 were dosed directly from the pure standard.

Histopathology

Fresh larvae were fixed for 24 hours in Duboscq-Brazil solution, dehydrated with a graded series of ethanol, diaphanized in xylene, imbedded in Paraplast Plus® (Sigma) and cut into sections 7 μm thick. Sections obtained from whole larvae were stained with haematoxylin and eosin for light microscopic analyses. The histology preparation was performed in the Laboratory of Reproduction and Community of Fish at UFPR.

Images were acquired under a light microscope (Scope.A1, Carl Zeiss, Germany) using a digital camera (AxioCam ERc5s, Carl Zeiss) and processed with Axion Vision SE64 software. Of the ten larvae exposed to each PBDE concentration, five were analysed. Of the control replicates, in water and solvent, also five of each were analysed, amounting to a total of 55 larvae analysed. Images of the exposed larvae were compared with those of the control treatments (water and solvent) as well as with those of the literature. A binomial test was used to assess the presence or absence of cell alterations. Significance level was set at 95%. Data were processed using BioEstat version 5.0 software (Ayres et al., 2005Ayres, M., Ayres Junior, M., Ayres, D., Santos, A., 2005. BioEstat 3.0: aplicações estatísticas nas áreas das ciências biológicas e médicas, ONG Mamiraua, Belém.).

Results

The concentrations of PBDEs used in the experiment did not cause mortality to the fourth instar C. sancticaroli larvae. All concentrations of the test solutions were within 10% variation with respect to the nominal values.

The structures that evidenced some alteration after exposure to BDE-17, BDE-47 and BDE-99 were oenocytes, Cuénot cells, midgut regions and salivary glands. None of the larvae from water or solvent controls exhibited any cell alteration.

Larval oenocytes showed changes such as vacuolisation of the cytoplasm (Fig. 1). The BDE-17 caused this type of alteration in 20% of the larvae exposed at 0.5 and 20 μg L-1, whereas the concentration 2.0 μg L-1 caused alteration in 60% of the observed larvae (X2 = 5.06, df=1, p=0.167). The BDE-47 caused alteration in 40% of the larvae exposed to the three concentrations (X2 = 3.46, p= 0.325), and the oenocytes of the larvae exposed to the different concentrations of BDE-99 did not present alterations (X2 = 6.66, df = 1, p=0.083) (Table 1).

Figure 1
Micrographs of oenocytes and Cuenot cells of Chironomus sancticaroli larvae after PBDE exposure. A. Oenocytes of control (water). B. Oenocytes exposed to BDE-17 at 20 μg L-1. C. Oenocytes exposed to BDE-47 at 2.0 μg L-1. Arrows show cytoplasm vacuolization. D. Cuénot cells of control (water). E. Cuénot cells exposed to BDE 17 at 20 μg L-1. F. Cuenot cells exposed to BDE 47 at 2.0 ug L-1. G. Cuenot cells exposed to BDE 99 at 0.5 μg L-1. Arrows show the brush border disruption and displacement in the apex cell. tr: trophocytes, cu: cutile, cc: Cuénot cells, oe: esophagus, cg: gastric caeca. Scale bar: 20 µm.
Table 1
Percentage of cell damage of Chironomus sancticarolli after 48h of exposure to BDE-17, BDE-47 and BDE-99 at three different concentrations.

The Cuénot cells displayed disruption and displacement in the apex brush border (Fig. 1). These alterations were observed in 40% of the larvae exposed to BDE-17 at 20 μg L-1(X2=5.6, df=1, p=0.132). Equally, larvae treated with BDE-99 at 0.5 μg L-1 and 2.0 μg L-1 presented the same changes in the apex brush border (X2=4.53, df=1, p=0.209), whereas BDE-47 at 2.0 μg L-1 caused a significant alteration in 60% of the exposed larvae (X2=8.66, df=1, p=0.034).

Midgut cells exhibited changes in the morphology of the apex cells located near the lumen of region I (Fig. 2). This change was observed in 20% and 40% of larvae exposed to BDE-17 at 0.5 μg L-1 and 2.0 μg L-1 respectively (X2=4.0 df=1, p=0.261). Similarly, BDE-47 at 0.5 μg L-1 and 2.0 μg L-1 caused changes in 40% of exposed larvae (X2=3.46, df=1, p=0.325). On the other hand, BDE-99 did not cause changes in the morphology cells of region I of the midgut but induced narrowing of the lumen diameter in 20% of the larvae exposed exclusively at 0.5 μg L-1 (X2=5.06, df=1, p=0.167) (Fig. 2). Furthermore, the midgut region II exhibited cytoplasmic vacuolisation in 60% of the larvae exposed at 2.0 μg L-1 of BDE-47 while BDE-99 at 20 μg L-1 induced vacuolisation of the cytoplasm in 40% of the exposed larvae (X2=5.6, df =1, p=0.133) (Fig. 2) (Table 1).

Figure 2
Micrographs of larval Chironomus sancticaroli midgut after acute exposition to PBDEs A. Region I midgut lumen belonging to control treatment (water). B. Region I midgut lumen exposed to BDE-99 at 0.5 μg L-1 exhibiting its narrowing. C. Epithelial cells of midgut, region I, exposed to BDE 47 at 0.5 μg L-1 showing changes in cell morphology. D Midgut cells, region II, of control treatment (water). E Midgut cells, region II, exposed to BDE-47 at 2.0 μg L-1 showing the cytoplasm vacuolization. Bars shows the width of the lumen. gc: gastric cecum. ep: gut epithelia. lu: lumen. sv: stomodeal valve. Scale bar: 20 µm.

The salivary glands were altered showing acidophilic granules in their cytoplasm. These granules were observed in 60% of the larvae exposed to BDE-17 at 0.5 μg L-1 and 20 μg L-1 (X2 = 9.86, df = 1, p = 0.019). BDE-47 also induced formation of granules in 40% of the larvae exposed at 0.5 and 2.0 μg L-1 respectively (X2 = 5.86, df = 1, p = 0.11) (Fig. 3) (Table 1).

Figure 3
Micrographs of the salivary gland of larval Chironomus sancticaroli after acute exposition to PBDEs A. Salivary gland of control treatment (water). B. Salivary gland exposed to BDE 47 at 0.5 μg L-1 showing formation of the cytoplasm acidophilic granules. C. Salivary gland exposed to BDE 17 at 20 μg L-1 shows formation of the cytoplasm acidophilic granules. Arrow. Scale bar: 20 µm.

No histopathological changes in the Malpighian tubules of the C. sancticaroli larvae were observed as an influence of the acute PBDEs exposure.

Discussion

Histological analysis revealed injuries in the diverse tissues of C. sancticaroli larvae after exposure to PBDE in acute conditions. Some of the most sensitive structures observed were the oenocytes, the BDE-17 and BDE-47 standing out in particular at each tested concentration that prompted cytoplasmic vacuolisation and alterations of the oenocytes format. These alterations might modify larval growth due to physiological functions in which oenocytes are involved. Furthermore, oenocytes that are injured might trigger the larval dispersal syndrome and reduce feeding as they affect lipids, increasing haemolymph as described in larvae of Drosophila melanogaster Meigen, 1830 (Gutierrez et al., 2007Gutierrez, E., Wiggins, D., Fielding, B., Gould, A. P., 2007. Specialized hepatocyte-like cells regulate Drosophila lipid metabolism. Nature 445, 275-280. https://doi.org/10.1038/nature05382.
https://doi.org/10.1038/nature05382...
). The injuries caused to chironomid oenocytes can be correlated with lipophilicity of PBDEs towards lipid-rich structures (ATSDR, 2004ATSDR, 2004. Toxicological Profile for Polybrominated Biphenyl and Polybrominated Diphenyl Ethers, Department of Health and Human Services. Atlanta, Georgia, pp. 1-564.) and their role of defence of the organism as the first structure affected in the presence of xenobiotics as described in Bombus morio (Swederus, 1787) (Hymenoptera: Apidae) (Abdalla & Domingues, 2015Abdalla, F. C., Domingues, C. E. C., 2015. Hepato-Nephrocitic System: A novel model of biomarkers for analysis of the ecology of stress in environmental biomonitoring. PLoS One. 10 (7), e0132349. https://doi.org/10.1371/journal.pone.0132349.
https://doi.org/10.1371/journal.pone.013...
).

BDE-99 did not induce alterations in the larvae’s oenocytes despite its known toxic effects, this fact can be explained in part due to the specific debromination (bromine loss) throughout the metabolic pathway of PBDEs which influences their toxicity and bioaccumulation rate (Roberts et al., 2011Roberts, S. C., Noyes, P. D., Gallagher, E. P., Stapleton, H. M., 2011. Species-specific differences and structure-activity relationships in the debromination of PBDE congeners in three fish species. Environ. Sci. Technol. 45 (5), 1999-2005. https://doi.org/10.1021/es103934x.
https://doi.org/10.1021/es103934x...
; Stapleton et al., 2004Stapleton, H. M., Letcher, R. J., Li, J., Baker, J. E., 2004. Dietary accumulation and metabolism of polybrominated diphenyl ethers by juvenile carp (Cyprinus carpio). Environ. Toxicol. Chem. 23, 1939-1946.; Usenko et al., 2013Usenko, C. Y., Robinson, E. M., Bruce, E. D., Usenko, S., 2013. Uptake and metabolism of individual polybrominated diphenyk ether congeners by embryonic zebrafish. Environ. Toxicol. Chem. 32 (5), 1153-1160. https://doi.org/10.1002/etc.2163.
https://doi.org/10.1002/etc.2163...
). It is probable that C. sancticaroli larvae transform BDE-99 to less brominated congeners such as BDE-47 or BDE-17 via metabolic pathways, as demonstrated in fish species (Roberts et al., 2011Roberts, S. C., Noyes, P. D., Gallagher, E. P., Stapleton, H. M., 2011. Species-specific differences and structure-activity relationships in the debromination of PBDE congeners in three fish species. Environ. Sci. Technol. 45 (5), 1999-2005. https://doi.org/10.1021/es103934x.
https://doi.org/10.1021/es103934x...
) or chemical models (Gandhi et al., 2006Gandhi, N., Bhavsar, S. P., Gewurtz, S. B., Diamond, M. L., Evenset, A., Christensen, G. N., Gregor, D., 2006. Development of a multichemical food web model: application to PBDEs in Lake Ellasjoen, Bear Island, Norway. Environ. Sci. Technol. 40 (15), 4714-4721.).

Disruption of the brush border of Cuénot cells was observed in larvae exposed to the three PBDE congeners, being the most noteworthy alteration in larvae exposed to BDE-47 at 2.0 μg L-1. The injury to the Cuénot cells structure by PBDEs can compromise the insect gut physiology as a consequence of failure in the production of the peritrophic matrix that protects the epithelium from mechanical abrasion (Agrawal et al., 2014Agrawal, S., Kelkenberg, M., Begum, K., Steinfeld, L., Williams, C. E., Kramer, K. J., Beeman, R. W., Park, Y., Muthukrishnan, S., Merzendorfer, H., 2014. Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut. Insect Biochem. Mol. Biol. 49, 24-34. https://doi.org/10.1016/J.IBMB.2014.03.009.
https://doi.org/10.1016/J.IBMB.2014.03.0...
; Tellam, 1996Tellam, R. L., 1996. The peritrophic matrix. In: Lehane, M.J., Billingsley, P.F. (Eds.), Biology of the Insect Midgut. Chapman & Hall, London, pp. 86-114.; Terra, 2001Terra, W. R. 2001. The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch. Insect Biochem. Physiol. 47, 47-61. https://doi.org/10.1002/arch.1036.
https://doi.org/10.1002/arch.1036...
). Moreover, the transport of ions, nutrients, water and digestive enzymes (Zhuzhikov, 1964Zhuzhikov, D. P. 1964. Function of the peritrophic membrane in Musca domestica L. and Calliphora erythrocephala Meig. J. Insect Physiol. 10, 273-278. https://doi.org/10.1016/0022-1910(64)90011-3.
https://doi.org/10.1016/0022-1910(64)900...
), as well as inactivation of ingested toxins (Hegedus et al., 2009Hegedus, D., Erlandson, M., Gillott, C., Toprak, U., 2009. New insights into peritrophic matrix synthesis, architecture, and function. Annu. Rev. Entomol. 54, 285-302. https://doi.org/10.1146/annurev.ento.54.110807.090559.
https://doi.org/10.1146/annurev.ento.54....
), can also be altered in the larvae.

The midgut of C. sancticaroli larvae showed variation in the morphology of the apex cells located next to the lumen after BDE-17 and BDE-47 exposure. BDE-99 produced the narrowing of the larvae lumen in region I and BDE-47 and BDE-99 caused cytoplasmic vacuolisation of region II of the larvae midgut. This vacuolisation was more evident in the larvae exposed to BDE-47. Cell alteration in region II of the midgut was not observed. The cytoplasmic vacuolisation observed can be associated with an imbalance of the osmotic process as recognised in larvae of Aedes aegypti (Linnaeus, 1762) after exposure to Annona coriacea Mart. (Annonaceae) and Schinus terebinthifolius Raddi (Anacardiaceae) extracts (Costa et al., 2012Costa, M., Pinheiro, D., Serrão, J., Pereira, M., 2012. Morphological changes in the midgut of Aedes aegypti L. (Diptera: Culicidae) larvae following exposure to an Annona coriacea (Magnoliales: Annonaceae) extract. Neotrop. Entomol. 41 (4), 311-314. https://doi.org/10.1007/s13744-012-0050-z.
https://doi.org/10.1007/s13744-012-0050-...
; Procópio et al., 2015Procópio, T. F., Fernandes, K. M., Pontual, E. V., Ximenes, R. M., Oliveira, A. R. C., Souza, C. S., Melo, A. M. M. A., Navarro, D. M. A. F., Paiva, P. M. G., Martins, G. F., Napoleão, T. H., 2015. Schinus terebinthifolius leaf extract causes midgut damage, interfering with survival and development of Aedes aegypti larvae. PLoS One 10 (5), 1-19. https://doi.org/10.1371/journal.pone.0126612.
https://doi.org/10.1371/journal.pone.012...
). Similarly, larvae of Ceraeochrysa claveri (Navás, 1911) also displayed vacuoles in the cytoplasm after neem oil intake (Scudeler & Santos, 2013Scudeler, E. L., Santos, D. C., 2013. Effects of neem oil (Azadirachta indica A. Juss) on midgut cells of predatory larvae Ceraeochrysa claveri (Navás, 1911) (Neuroptera: chrysopidae). Micron 44, 125-132. https://doi.org/10.1016/j.micron.2012.05.009.
https://doi.org/10.1016/j.micron.2012.05...
). At the same time, cytoplasm vacuolisation can be caused by synthetic insecticides targeting ion channel proteins as reported in Culex quinquefasciatus Say, 1823 (Alves et al., 2010Alves, S. N., Serrão, J. E., Melo, A. L., 2010. Alterations in the fat body and midgut of Culex quinquefasciatus larvae following exposure to different insecticides. Micron. 41 (6), 592-597. https://doi.org/10.1016/j.micron.2010.04.004.
https://doi.org/10.1016/j.micron.2010.04...
) and compounds that interact with the nicotinic acetylcholine receptors in the nervous system as described in Apis mellifera Linnaeus, 1758 (Catae et al., 2014Catae, A. F., Roat, T. C., Oliveira, R. A., Ferreira Nocelli, R. C., Malaspina, O., 2014. Cytotoxic effects of thiamethoxam in the midgut and malpighian tubules of Africanized Apis mellifera (Hymenoptera: apidae). Microsc. Res. Tech. 77 (4), 274-281. https://doi.org/10.1002/jemt.22339.
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; Kakamand et al., 2008Kakamand, F.A.K., Mahmoud, T.T., Amin, A.-B.M., 2008. The role of three insecticides in disturbance the midgut tissue in honey bee Apis mellifera L. workers. J. Dohuk Univ. 11 (1), 144-151.).

Salivary glands exhibited granule formation in the cytoplasm prompted by BDE-17 and BDE-47 characterised by a high eosin affinity indicating its acid nature. Salivary glands of larvae exposed to BDE-17 exhibited more granules than those exposed to BDE-47. The present study describes for the first time the acid grains growth in chironomid salivary glands. Some alterations reported in the salivary glands of insects encompass the disruption of the membrane cells, cytoplasm vacuolisation and nuclear deformation after exposure to neonicotinoids in Musca domestica Linnaeus, 1758 (Mohammed Xider, 2018Mohammed Xider, K. 2018. Histopathological and morphological alterations in salivary gland of House fly induced by oral administration Thiamethoxam. Kurd. J. Appl. Res. 3 (1), 40-44. https://doi.org/10.24017/science.2018.1.8.
https://doi.org/10.24017/science.2018.1....
). In addition to cellular modifications caused by the direct ingestion of xenobiotics, the capacity of salivary glands to remove substances from the haemolymph that were not eliminated by the Malpighian tubules can also compromise the cellular integrity of the glands (Armbruster et al., 1986Armbruster, L., Levy, M., Mathieu, M. N., Bautz, A. M., 1986. Acid phosphatase activity in the hemolymph, hemocytes, fat body and salivary glands during larval and prepupal development in Calliphora erythrocephala (Diptera: Calliphoridae). Comp. Biochem. Physiol. Part B Comp. Biochem. 84 (3), 349-354. https://doi.org/10.1016/0305-0491(86)90088-X.
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; Meirelles et al., 2001Meirelles, R. M., Silva, E. C., Silva de Moraes, R. L., 2001. Lipid distribution in salivary glands of larvae and adult bees (Hymenoptera: apidae). Cytobios 106 (Suppl.1), 57-66.). Moreover, failures in silk production can compromise the anti-predator function of tubes and compromise the survival of individuals (Dillon, 1985Dillon, P. M. 1985. Chironomid larval size and case presence influence capture success achieved by dragonfly larvae. Freshw. Invertebr. Biol. 4, 22-29. https://doi.org/10.2307/1467195.
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; Hershey, 1987Hershey, A. E. 1987. Tubes and foraging behavior in larval Chironomidae: implications for predator avoidance. Oecologia 73 (2), 236-241. https://doi.org/10.1007/BF00377513.
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).

Our study did not detect any alterations in the Malpighian tubule cells as an effect of the PBDE exposure. The maintenance of the integrity may be correlated with the presence of a large quantity of mitochondria, which means that cells are very active (Chapman, 2013Chapman, R. F., 2013. Excretion and salt and water regulation. In: Simpson, S., Douglas, A. (Eds.), The Insects: Structure and Function. Cambridge University Press, New York, pp. 546-584.) and rich in genes, expressed in this organ, that are responsible for regulating enzymes like glutathione S-transferase and Cytochrome P450 as described in Drosophila (Wang et al., 2004Wang, J., Kean, L., Yang, J., Allan, A. K., Davies, S. A., Herzyk, P., Dow, J. A., 2004. Function-informed transcriptome analysis of Drosophila renal tubule. Genome Biol. 5 (9), R69. https://doi.org/10.1186/gb-2004-5-9-r69.
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). These enzymes are involved in the metabolism and detoxification of toxic substances present in organisms (Boelsterli, 2007Boelsterli, U. A. 2007. Mechanistic Toxicology: The Molecular Basis of How Chemicals Disrupt Biological Targets, 2nd ed. CRC Press, Boca Raton.). It was demonstrated that BDE-17, -47 and -99 at concentrations ranging from 0.5 to 3 μg L-1 caused an increase of the glutathione S-transferase activity of the C. sancticaroli larvae (Palacio-Cortés et al., 2017Palacio-Cortés, A. M., Signorini-Souza, I. D. L., Yoshio Hara, E. L., Disner, R. G., Rebechi, D., Grassi, M. T., Cestari, M. M., Navarro-Silva, M. A., 2017. Polybrominated diphenyl ethers (PBDEs) effects on Chironomus sancticaroli larvae after short-term exposure. Ecotoxicol. Environ. Saf. 139, https://doi.org/10.1016/j.ecoenv.2017.01.052.
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).

Despite histological alterations which commonly provide powerful tools for distinguishing and describing the long-term effects of environmental contaminants (Ben Ameur et al., 2015Ben Ameur, W., El Megdiche, Y., de Lapuente, J., Barhoumi, B., Trabelsi, S., Ennaceur, S., Camps, L., Serret, J., Ramos-López, D., Gonzalez-Linares, J., Touil, S., Driss, M. R., Borràs, M., 2015. Oxidative stress, genotoxicity and histopathology biomarker responses in Mugil cephalus and Dicentrarchus labrax gill exposed to persistent pollutants. A field study in the Bizerte Lagoon: Tunisia. Chemosphere. 135, 67-74. https://doi.org/10.1016/J.CHEMOSPHERE.2015.02.050.
https://doi.org/10.1016/J.CHEMOSPHERE.20...
; Liney et al., 2006Liney, K. E., Hagger, J. A., Tyler, C. R., Depledge, M. H., Galloway, T. S., Jobling, S., 2006. Health effects in fish of long-term exposure to effluents from wastewater treatment works. Environ. Health Perspect. 114, 81-89. https://doi.org/10.1289/ehp.8058.
https://doi.org/10.1289/ehp.8058...
; Schwaiger et al., 2000Schwaiger, J., Spieser, O. H., Bauer, C., Ferling, H., Mallow, U., Kalbfus, W., Negele, R. D., 2000. Chronic toxicity of nonylphenol and ethinylestradiol: haematological and histopathological effects in juvenile Common carp (Cyprinus carpio). Aquat. Toxicol. 51, 69-78.), the current study detected histopathologic lesions of PBDEs in C. sancticaroli larvae in short-term exposure. In conclusion, this study demonstrates that BDE-17, BDE-47 and BDE-99 in an in vivo model induced histological alterations along the evaluated concentrations. This paper contributes to the knowledge of the effects of PBDEs in cell structures of the Chironomus sancticaroli larvae as biomonitoring species of sediment systems.

Acknowledgements

This work was supported by the cooperation program between Newton Fund, Conselho Nacional das Fundações Estaduais de Amparo à Pesquisa – Fundação Araucária (Grant number 45191.460.30251.29012015); the National Counsel of Technological and Scientific Development (Grant numbers 307916/2016-2). I.L. Signorini-Souza is grateful to Fundação Araucária for the fellowship.

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Edited by

Associate Editor: Maria Anice Sallum

Publication Dates

  • Publication in this collection
    17 Jan 2020
  • Date of issue
    2020

History

  • Received
    22 May 2019
  • Accepted
    13 Oct 2019
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